Abstract
Available guidance to mitigate health risks from exposure to freshwater harmful algal blooms (HABs) is largely derived from temperate ecosystems. Yet in tropical ecosystems, HABs can occur year-round, and resource-dependent populations face multiple routes of exposure to toxic components. Along Winam Gulf, Lake Victoria, Kenya, fisher communities rely on lake water contaminated with microcystins (MCs) from HABs. In these peri-urban communities near Kisumu, we tested hypotheses that MCs exceed exposure guidelines across seasons, and persistent HABs present a chronic risk to fisher communities through ingestion with minimal water treatment and frequent, direct contact. We tested source waters at eleven communities across dry and rainy seasons from September 2015 through May 2016. We measured MCs, other metabolites, physicochemical parameters, chlorophyll-a, phytoplankton abundance and diversity, and fecal indicators. We then selected four communities for interviews about water sources, usage, and treatment. Greater than 30% of source water samples exceeded WHO drinking water guidelines for MCs (1 µg/L), and over 60% of source water samples exceeded USEPA guidelines for children and immunocompromised individuals. 50% of households reported a sole source of raw lake water for drinking and household use, with alternate sources including rain and boreholes. Household chlorination was the most widespread treatment utilized. At this tropical, eutrophic lake, HABs pose a year-round health risk for fisher communities in resource -limited settings. Community-based solutions and site-specific guidance for Kisumu Bay and similarly impacted regions is needed to address a chronic health exposure likely to increase in severity and duration with global climate change.
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References
APHA (American Public Health Association), AWWA (American Water Works Association), WEF (World Economic Forum) (2017) 9223 Enzyme Substrate Coliform Test. In: Standard Methods for the Examination of Water and Wastewater, 23rd edn. https://doi.org/10.2105/SMWW.2882.194
Bhateria R, Jain D (2016) Water quality assessment of lake water: a review. Sustain Water Resour Manag 2:161–173. https://doi.org/10.1007/s40899-015-0014-7
Bain R, Cronk R, Wright J, Yang H, Slaymaker T, Bartram J (2014) Fecal contamination of drinking-water in low- and middle-income countries: a systematic review and meta-analysis. PLoS Med 11:e1001644. https://doi.org/10.1371/journal.pmed.1001644
Beversdorf LJ, Weirich CA, Bartlett SL, Miller TR (2017) Variable cyanobacterial toxin and metabolite profiles across six eutrophic lakes of differing physiochemical characteristics. Toxins (Basel) 9(2):62. https://doi.org/10.3390/toxins9020062
Beversdorf LJ, Rude K, Weirich CA, Bartlett SL, Seaman M, Kozik C et al (2018) Analysis of cyanobacterial metabolites in surface and raw drinking waters reveals more than microcystin. Water Res 140:280–290. https://doi.org/10.1016/j.watres.2018.04.032
Carlson RE (1977) A trophic index for lakes. Limnol Oceanogr 22(2):361–369
Chen J, Xie P, Li L, Xu J (2009) First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage. Toxicol Sci 108:81–89. https://doi.org/10.1093/toxsci/kfp009
Codd GA, Morrison LF, Metcalf JS (2005) Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203:264–272. https://doi.org/10.1016/j.taap.2004.02.016
Corbel S, Mougin C, Bouaicha N (2014) Cyanobacterial toxins: modes of actions, fate in aquatic and soil ecosystems, phytotoxicity and bioaccumulation in agricultural crops. Chemosphere 96:1–15. https://doi.org/10.1016/j.chemosphere.2013.07.056
Faltermann S, Zucchi S, Kohler E, Blom JF, Pernthaler J, Fent K (2014) Molecular effects of the cyanobacterial toxin cyanopeptolin (cp1020) occurring in algal blooms: global transcriptome analysis in zebrafish embryos. Aquat Toxicol 149:33–39. https://doi.org/10.1016/j.aquatox.2014.01.018
FAO (Food and Agriculture Organization of the United Nations) (2014) The State of World Fisheries and Aquaculture 2014. FAO, Rome, p 223. https://www.fao.org/3/a-i3720e.pdf. Accessed 5 June 2018
Fiorella KJ, Seto K, Gavenus E, Milner EM, Omollo DO, Mattah B, Fenald LCH, Brashares J (2016) Examining local fish consumption in the globalized Lake Victoria fishery. FASEB J 30 (1, supplement):100000. DOI: 10.1096/fasebj.30.1_supplement.894.4.
Fiorella KJ, Milner EM, Salmen CR, Hickey MD, Omollo DO, Odhiambo A, Mattah B, Bukusi EA, Fernald LCH, Brashares JS (2017) Human health alters the sustainability of fishing practices in East Africa. Proc Natl Acad Sci USA 114:4171–4176. https://doi.org/10.1073/pnas.1613260114
Ford L, Bharadwaj L, Mcleod L, Waldner C (2017) Human health risk assessment applied to rural populations dependent on unregulated drinking water sources: a scoping review. Int J Environ Res Public Health 14(8):846. https://doi.org/10.3390/ijerph14080846
Funari E, Testai E (2008) Human health risk assessment related to cyanotoxins exposure. Crit Rev Toxicol 38:97–125. https://doi.org/10.1080/10408440701749454
Haande S, Thomas R, Semyalo RP, Brettum P, Edvardsen B, Lyche-Solheim A, Sorensen K, Larsson P (2011) Phytoplankton dynamics and cyanobacterial dominance in Murchison Bay of Lake Victoria (Uganda) in relation to environmental conditions. Limnologica Ecol Manag Inland Waters 41:20–29. https://doi.org/10.1016/j.limno.2010.04.001
Hecky RE, Mugidde R, Ramlal PS, Talbot MR, Kling GW (2010) Multiple stressors cause rapid ecosystem change in Lake Victoria. Freshw Biol 55:19–42. https://doi.org/10.1111/j.1365-2427.2009.02374.x
Herrie T, Plummer S, Roberson JA (2017) Occurrence and state approaches for addressing cyanotoxins in US drinking water. J Am Water Works Assoc 109:40–47. https://doi.org/10.5942/jawwa.2017.109.0022
Hilborn ED, Beasley VR (2015) One health and cyanobacteria in freshwater systems: animal illnesses and deaths are sentinel events for human health risks. Toxins (Basel) 7:1374–1395. https://doi.org/10.3390/toxins7041374
Ibelings BW, Backer LC, Kardinaal WE, Chorus I (2015) Current approaches to cyanotoxin risk assessment and risk management around the globe. Harmful Algae 49:63–74. https://doi.org/10.1016/j.hal.2014.10.002
Jonas A, Scholz S, Fetter E, Sychrova E, Novakova K, Ortmann J, Benisek M, Adamovsky O, Giesy JP, Hilscherova K (2015) Endocrine, teratogenic and neurotoxic effects of cyanobacteria detected by cellular in vitro and zebrafish embryos assays. Chemosphere 120:321–327. https://doi.org/10.1016/j.chemosphere.2014.07.074
Kenya HIV County Profiles (2016) Ministry of Health. National AIDS Control Council, 1–238. https://nacc.or.ke/wp-content/uploads/2016/12/Kenya-HIV-County-Profiles-2016.pdf. Accessed 01 June 2018
Kundu R, Aura CM, Nyameweya C, Agembe S, Sitoki L, Lung'ayia H, Ongore C, Ogari Z, Werimo K (2017) Changes in pollution indicators in Lake Victoria, Kenya and their implications for lake and catchment management. Lakes Reserv Res Manag 22:199–214. https://doi.org/10.1111/lre.12187
Kwena ZA, Bukusi E, Omondi E, Ng'ayo M, Holmes KK (2012) Transactional sex in the fishing communities along Lake Victoria, Kenya: a catalyst for the spread of HIV. Afr J AIDS Res 11:9–15. https://doi.org/10.2989/16085906.2012.671267
Lenz KA, Miller TR, Ma H (2018) Anabaenopeptins and cyanopeptolins induce systemic toxicity effects in a model organism the nematode Caenorhabditis elegans. Chemosphere 214:60–69. https://doi.org/10.1016/j.chemosphere.2018.09.076
Li Y, Chen JA, Zhao Q, Pu C, Qiu Z, Zhang R, Shu W (2011) A cross-sectional investigation of chronic exposure to microcystin in relationship to childhood liver damage in the Three Gorges Reservoir region, China. Environ Health Perspect 119:1483–1488. https://doi.org/10.1289/ehp.1002412
Li P, Feng W, Xue C, Tian R, Wang S (2017) Spatiotemporal variability of contaminants in lake water and their risks to human health: a case study of the Shahu Lake tourist area, northwest China. Expo Health 9(3):213–225. https://doi.org/10.1007/s12403-016-0237-3
Liyanage HM, Arachchi DN, Abeysekara T, Guneratne L (2016) Toxicology of freshwater cyanobacteria. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 34:137–168. https://doi.org/10.1080/10590501.2016.1193923
Lung'ayia H, Sitoki L, Kenyanya M (2001) The nutrient enrichment of Lake Victoria (Kenyan waters). Hydrobiologia 458:75–82. https://doi.org/10.2478/v10102-009-0006-2
Massey IY, Yang F, Ding Z, Yang S, Guo J, Tezi C, Alosman M, Kamegni RB, Zeng W (2018) Exposure routes and health effects of microcystins on animals and humans: a mini-review. Toxicon 151:156–162. https://doi.org/10.1016/j.toxicon.2018.07.010
Mbonde A, Sitoki L, Kurmayer R (2015) Phytoplankton composition and microcystin concentrations in open and closed bays of Lake Victoria, Tanzania. Aquat Ecosyst Health Manag 18:212–220. https://doi.org/10.1080/14634988.2015.1011030
Mello FD, Braidy N, Marcal H, Guillemin G, Nabavi SM, Neilan BA (2018) Mechanisms and effects posed by neurotoxic products of cyanobacteria/microbial eukaryotes/dinoflagellates in algae blooms: a review. Neurotox Res 33:153–167. https://doi.org/10.1007/s12640-017-9780-3
Merel S, Villarin MC, Chung K, Snyder S (2013) Spatial and thematic distribution of research on cyanotoxins. Toxicon 76:118–131. https://doi.org/10.1016/j.toxicon.2013.09.008
Minakawa N, Dida GO, Sonye GO, Futami K, Njenga SM (2012) Malaria vectors in Lake Victoria and adjacent habitats in Western Kenya. PLoS ONE 7:e32725. https://doi.org/10.1371/journal.pone.0032725
Mowe M, Mirovic S, Lim RP, Furey A, Yeo D (2015) Tropical cyanobacterial blooms: a review of prevalence, problem taxa, toxins and influencing environmental factors. J Limnol 74:205–224. https://doi.org/10.4081/jlimnol.2014.1005
Nagata JM, Fiorella KJ, Salmen CR, Hickey MD, Mattah B, Magerenge R, Milner E, Weiser SD, Bukusi EA, Cohen CR (2015) Around the table: Food insecurity, socioeconomic status, and instrumental social support among women living in a rural Kenyan island community. Ecol Food Nutr 54:358–369. https://doi.org/10.1080/03670244.2014.995790
Ngure FM, Reid BM, Humphrey JH, Mbuya MN, Pelto G, Stoltzfus RJ (2014) Water, sanitation, and hygiene (wash), environmental enteropathy, nutrition, and early child development: making the links. Ann N Y Acad Sci 1308:118–128. https://doi.org/10.1111/nyas.12330
Nyakairu GW, Nagawa CB, Mbabazi J (2010) Assessment of cyanobacteria toxins in freshwater fish: a case study of Murchison Bay (Lake Victoria) and Lake Mburo, Uganda. Toxicon 55:939–946. https://doi.org/10.1016/j.toxicon.2009.07.024
Ofulla AV, Adoka SO, Anyona DN, Abuom PO, Karanja DM, Vulule JM, Okurut T, Matano A, Dida GO, Jembe T, Gichuki J (2013) Spatial distribution and habitat characterization of schistosomiasis host snails in lake and land habitats of Western Kenya. Lakes Reserv 18:197–215. https://doi.org/10.1111/lre.12032
Omwega RN, Abila RO, Lwenya C (2006) Fishing and poverty levels around Lake Victoria (Kenya). In: Odada E, Olago DO (eds) Proceedings of the 11th world lakes conference, vol 2, pp. 193–199. https://hdl.handle.net/1834/1495
Otieno FO, Ndivo R, Oswago S, Magerenge R (2015) Correlates of prevalent sexually transmitted infections among participants screened for an HIV incidence cohort study in Kisumu, Kenya. Int J STD AIDS 26:225–237. https://doi.org/10.1177/0956462414532447
Paerl HW (2018) Mitigating toxic planktonic cyanobacterial blooms in aquatic ecosystems facing increasing anthropogenic and climatic pressures. Toxins (Basel) 10(2):E76. https://doi.org/10.3390/toxins10020076
Pham TL, Utsumi M (2018) An overview of the accumulation of microcystins in aquatic ecosystems. J Environ Manage 213:520–529. https://doi.org/10.1016/j.jenvman.2018.01.077
Poste AE, Hecky RE, Guildford SJ (2011) Evaluating mi crocystin exposure risk through fish consumption. Environ Sci Technol 45:5806–5811. https://doi.org/10.1021/es200285c
Qian H, Liu G, Lu T, Sun L (2018) Developmental neurotoxicity of microcystis aeruginosa in the early life stages of zebrafish. Ecotoxicol Environ Saf 151:35–41. https://doi.org/10.1016/j.ecoenv.2017.12.059
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/.
Rastogi RP, Madamwar D, Incharoensakdi A (2015) Bloom dynamics of cyanobacteria and their toxins: environmental health impacts and mitigation strategies. Front Microbiol 6:1254. https://doi.org/10.3389/fmicb.2015.01254
Roegner AF, Brena B, Gonzalez-Sapienza G, Puschner B (2014) Microcystins in potable surface waters: toxic effects and removal strategies. J Appl Toxicol 34:441–457. https://doi.org/10.1002/jat.2920
Saqrane S, Oudra B (2009) CyanoHAB occurrence and water irrigation cyanotoxin contamination: ecological impacts and potential health risks. Toxins 1(2):113–122. https://doi.org/10.3390/toxins1020113
Simiyu BM, Oduor SO, Rohrlack T, Sitoki L, Kurmayer R (2018) Microcystin content in phytoplankton and in small fish from eutrophic Nyanza Gulf, Lake Victoria. Kenya. Toxins (Basel) 10(7):275. https://doi.org/10.3390/toxins10070275
Sitoki L, Gikuchi J, Ezekiel C, Wanda F, Mkumbo O, Marshall B (2010) The environment of Lake Victoria (East Africa): current status and historical changes. Int Rev Hydrobiol 95:209–223. https://doi.org/10.1002/iroh.201011226
Sitoki L, Kurmayer R, Rott E (2012) Spatial variation of phytoplankton composition, biovolume, and resulting microcystin concentrations in the Nyanza Gulf (Lake Victoria, Kenya). Hydrobiologia 691:109–122. https://doi.org/10.1007/s10750-012-1062-8
Steffen MM, Davis TW, McKay RML, Bullerjahn GS, Krausfeldt LE, Stough JMA, Neitzey ML, Gilbert NE, Boyer GL, Johengen TH, Gossiaux DC, Burtner AM, Palladino D, Rowe MD, Dick GJ, Meyer KA, Levy S, Boone BE, Stumpf RP, Wynne TT, Zimba PV, Gutierrez D, Wilheim SW (2017) Ecophysiological examination of the Lake Erie Microcystis bloom in 2014: linkages between biology and the water supply shutdown of Toledo, OH. Environ Sci Technol 51:6745–6755. https://doi.org/10.1021/acs.est.7b00856
Stough JMA, Tang X, Krausfeldt LE, Steffen MM, Gao G, Boyer GL et al (2017) Molecular prediction of lytic v.s. lysogenic states for Microcystis phage: metatranscriptomic evidence of lysogeny during large bloom events. PLoS ONE 12:e0184146. https://doi.org/10.1371/journal.pone.0184146
Svircev Z, Drobac D, Tokodi N, Mijovic B, Codd GA, Meriluoto J (2017) Toxicology of microcystins with reference to cases of human intoxications and epidemiological investigations of exposures to cyanobacteria and cyanotoxins. Arch Toxicol 91:621–650
USEPA (2015) Drinking Water Health Advisory for the Cyanobacterial Microcystin Toxins EPA-820R15100 Washington, DC. https://www.epa.gov/sites/production/files/2017-06/documents/microcystins-report-2015.pdf. Accessed 19 June 2016
Valderrama JC (1981) The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Mar Chem 21:109–122. https://doi.org/10.1016/0304-4203(81)90027-X
Walls JT, Wyatt KH, Doll JC, Rubenstein EM, Rober AR (2018) Hot and toxic: temperature regulates microcystin release from cyanobacteria. Sci Total Environ 610–611:786–795. https://doi.org/10.1016/j.scitotenv.2017.08.149
Weirich CA, Miller TR (2014) Freshwater harmful algal blooms: toxins and children’s health. Curr Probl Pediatr Adolesc Health Care 44:2–24. https://doi.org/10.1016/j.cppeds.2013.10.007
Westrick JA, Szlag DC, Southwell BJ, Sinclair J (2010) A review of cyanobacteria and cyanotoxins removal/inactivation in drinking water treatment. Anal Bioanal Chem 397:1705–1714
WHO (World Health Organization) (2003a) Emerging issues in water and infectious disease. WHO, Paris
WHO (2003b) Algae and cyanobacteria in fresh water. In: Guidelines for safe recreational water environments, vol 1: coastal and Fresh Waters. World Health Organization, Geneva, pp 1–219. www.who.int/water_ sanitation_health/bathing/srwg1.pdf
WHO (2017) Chemical fact sheets. In: Guidelines for drinking-water quality: 4th edn. Incorporating the First Addendum, Geneva, pp 307–441. License: CCBY-NC-SA 3.0 IGO. https://www.who.int/water_sanitation_health/publications/drinking-water-quality-guidelines-4-including-1st-addendum/en/
Wu J, Xue C, Tian R, Wang S (2017) Lake water quality assessment: a case study of Shahu Lake in the semi-arid loess area of northwest China. Environ Earth Sci 76:232. https://doi.org/10.1007/s12665-017-6516-x
Yoshida-Takashima Y, Yoshida M, Ogata H, Nagasaki K, Hiroishi S, Yoshida T (2012) Cyanophage infection in the bloom-forming cyanobacteria Microcystis aeruginosa in surface freshwater. Microbes Environ 27:350–355. https://doi.org/10.1264/jsme2.ME12037
Acknowledgements
The authors would like to thank staff, research, and interns at Kenya Marine and Fisheries Research Institute, and at the Research Care and Training Program (RCTP), Kenya Medical Research Institute (KEMRI). In particular, the fisherfolk outreach through Family AIDS Care and Education Services (FACES) was instrumental for approaching communities for sampling and interviews, and the authors would like to give special thanks to Dr. Zachary Kwena, David Ang’awa, Bernard Dajo, and Frederick Otieno.
Funding
The bulk of in-country work was supported by NIH Research Training Grant # R25 TW009343 funded by the Fogarty International Center and the University of California Global Health Institute (UCGHI). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH or the UCGHI. Laboratory work was funded in part by a Grant to TM from the National Institutes of Environmental Health Sciences, Oceans and Human Health, #1R01ES022075-01. Additional funding was provided through the University of Madison-Wisconsin Global Health Institute (GHI) Seed Grant, and the One Health Program at University of Nebraska-Lincoln provided postdoctoral funding for the first author during the writing of this manuscript.
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Supplemental Fig. 1 Routes of Exposure to MCs and Other Metabolites for Fisher Communities at Lake Victoria. In addition to oral intake via drinking water and accidental ingestion during recreation, other routes of exposure include dietary through substantial fish (daily), dermal contact, and possible other accumulation through the local environment and use (plant and animal products). Body weight, adsorption, distribution, metabolism, and excretion (ADME), and individual behaviors all mediate individual risk (PDF 12491 kb)
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Roegner, A., Sitoki, L., Weirich, C. et al. Harmful Algal Blooms Threaten the Health of Peri-Urban Fisher Communities: A Case Study in Kisumu Bay, Lake Victoria, Kenya. Expo Health 12, 835–848 (2020). https://doi.org/10.1007/s12403-019-00342-8
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DOI: https://doi.org/10.1007/s12403-019-00342-8